Small but Manifold - Hidden Diversity in "Spumella-like Flagellates"

Abstract

Colourless, nonscaled chrysophytes comprise morphologically similar or even indistinguishable flagellates which are important bacterivors in water and soil crucial for ecosystem functioning. However, phylogenetic analyses indicate a multiple origin of such colourless, nonscaled flagellate lineages. These flagellates are often referred to as "Spumella-like flagellates" in ecological and biogeographic studies. Although this denomination reflects an assumed polyphyly, it obscures the phylogenetic and taxonomic diversity of this important flagellate group and, thus, hinders progress in lineage- and taxon-specific ecological surveys. The smallest representatives of colourless chrysophytes have been addressed in very few taxonomic studies although they are among the dominant flagellates in field communities. To overcome the blurred picture and set the field for further investigation in biogeography and ecology of the organisms in question, we studied a set of strains of specifically small, colourless, nonscaled chrysomonad flagellates by means of electron microscopy and molecular analyses. They were isolated by a filtration-acclimatisation approach focusing on flagellates of around 5 μm. We present the phylogenetic position of eight different lineages on both the ordinal and the generic level. Accordingly, we describe the new genera Apoikiospumella, Chromulinospumella, Segregatospumella, Cornospumella and Acrispumella Boenigk et Grossmann n. g. and different species within them.

Keywords: Bacterivorous protists; Chrysomonads; Chrysophyceae; Monas; Stramenopiles; biodiversity; heterotrophic nanoflagellates; microbial food web; microbial loop; taxonomy.

Figure 1

Light microscopic images (A–P) showing vegetative cells of strains of colourless nonscaled chrysophytes. A. 199hm = Spumella vulgaris. B. 1006 = Pedospumella encystans. C. AR3A3 = Segregatospumella dracosaxi n. gen. n. sp. D. AR4A6 = Spumella rivalis. E. AR4D6 = Cornospumella fuschlensis n. gen. n. sp. F. JBAF33 = Acrispumella msimbaziensis n. gen. n. sp. G. JBC07 = Poteriospumella lacustris. H. JBC27 = Chromulinospumella sphaerica n. gen. nov. comb. I. JBCS23 = Pedospumella sinomuralis n.sp. J. JBL14 = Spumella bureschii nov. comb. K. JBM08 = Apoikiospumella mondseeiensis n. gen. n. sp. L. JBM10 = Poteriospumella lacustris. M. JBMS11 = Pedospumella encystans. N. JBNZ39 = Spumella lacusvadosi n. sp. O. JBNZ41 = Poteriospumella lacustris. P. N1846. Scale bars = 10 μm for (A–P).

Figure 2

TEM images (positive contrast) (A–DD) showing vegetative cells of strains of colourless nonscaled chrysophytes. Two images per strain are given respectively: 1. whole cell, 2. zoom on mastigonemes of large flagellum. A+B. JBL14 = Spumella bureschii nov. comb. C+D. 199hm = Spumella vulgaris. E+F. AR4D6 = Cornospumella fuschlensis n. gen. n. sp. G+H. JBCS23 = Pedospumella sinomuralis n. sp. I+J. 1006 = Pedospumella encystans. K+L. JBMS11 = Pedospumella encystans. M+N. AR4A6 = Spumella rivalis. O+P. JBC27 = Chromulinospumella sphaerica n. gen. nov. comb. Q+R. N1846. S+T. AR3A3 = Segregatospumella dracosaxi n. gen. n. sp. U+V. JBM10 = Poteriospumella lacustris. W+X. JBC07 = Poteriospumella lacustris. Y+Z. JBNZ41 = Poteriospumella lacustris. AA + BB . JBAF33 = Acrispumella msimbaziensis n. gen. n. sp. CC + DD . JBM08 = Apoikiospumella mondseeiensis n. gen. n. sp. Scale bars = 3 μm for (A, C, E, G, I, K, M, O, Q, S, U, W, Y, AA, CC). Scale bars = 1 μm for (B, D, F, H, J, L, N, P, R, T, V, X, Z, BB, DD).

Figure 3

TEM images (ultrathin sections) (A–F) showing cell interior of strains of colourless nonscaled chrysophytes. Core‐associated plastidal organells are highlighted. A. JBM10 = Poteriospumella lacustris. B. JBC07 = Poteriospumella lacustris. C. AR4D6 = Cornospumella fuschlensis n. gen. n. sp. D. JBNZ41 = Poteriospumella lacustris. E. 199hm = Spumella vulgaris. F. JBMS11 = Pedospumella encystans. Scale bars = 1 μm for (A–F).

Figure 4

Maximum‐likelihood phylogeny based on SSU sequences showing the investigated strains of colourless nonscaled chrysophytes (bolt print) within Chrysophyceae. Numbers at nodes give bootstrap values and posterior probabilities in following order: maximum‐likelihood/Bayesian/maximum‐parsimony/neighbour‐joining (values > 50 are shown; posterior probabilities > 0.95).

Figure 5

Maximum‐likelihood phylogeny based on 5.8S sequences of strains of colourless nonscaled chrysophytes. Numbers at nodes give bootstrap values and posterior probabilities in following order: maximum‐likelihood/Bayesian/maximum‐parsimony/neighbour‐joining (values > 50 are shown; posterior probabilities > 0.95). Two additional photosynthetic chrysophycean species (in green) show polyphyly of colourless nonscaled chrysophytes.

Figure 6

Maximum‐likelihood phylogeny based on LSU sequences of strains of colourless nonscaled chrysophytes. Numbers at nodes give bootstrap values and posterior probabilities in following order: maximum‐likelihood/Bayesian/maximum‐parsimony/neighbour‐joining (values > 50 are shown; posterior probabilities > 0.95). Two additional photosynthetic chrysophycean species (in green) show polyphyly of colourless nonscaled chrysophytes.

Figure 7

Maximum‐likelihood phylogeny based on COX1 sequences of strains of colourless nonscaled chrysophytes. Numbers at nodes give bootstrap values and posterior probabilities in following order: maximum‐likelihood/Bayesian/maximum‐parsimoy/neighbour‐joining (values > 50 are shown; posterior probabilities > 0.95). Two additional photosynthetic chrysophycean species (in green) show polyphyly of colourless nonscaled chrysophytes.